Skip to main content

Advertisement

SpringerLink
Log in

Antimicrobial resistance, genetic characterization, and molecular epidemiology of Ureaplasma species in males with infertility

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

This study aimed to study the antimicrobial resistance, genetic characterization, and molecular epidemiology of Ureaplasma species in order to provide clinicians sufficient data to select optimal strategies of treatment for genitourinary tract infections of infertile male patients. Firstly, a total of 817 clinical semen specimens were detected for Ureaplasma species by molecular detection. Secondly, culture and identification of Ureaplasma species were achieved by using Mycoplasma ICS Test, and the antimicrobial susceptibility tests were determined by using broth microdilution assay. Then, the tetracycline resistance genetic determinants in Ureaplasma species were identified by PCR, and the fluoroquinolone and macrolide resistance genetic determinants were identified by DNA sequencing. Finally, the molecular epidemiology of Ureaplasma species was studied by both multilocus sequence typing (MLST) and expanded MLST (eMLST) schemes. Among the 817 semen specimens, 320 (39.17%) specimens were positive for Ureaplasma species. The percentages of resistance in 320 isolates against LEV, MXF, TET, and ERY were 47.5%, 39.38%, 19.69%, and 3.75%, respectively. The tet(M) and int-Tn genes were detected positive in all the tetracycline-resistant isolates. One macrolide-resistant UU isolate had a novel amino acid alteration (R66T) in L4 ribosomal protein and another UU isolate harbored a novel alteration (S109T) in L22. In fluoroquinolone-resistant isolates, S83L substitution in the ParC was predominant. In this area, ST22 and eST16 were the most prevalent ST and eST, respectively. One ST and 3 eSTs were newly identified in this study. This study has demonstrated that ERY can be first-line therapy for Ureaplasma species infections.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Agarwal A, Rana M, Qiu E, AlBunni H, Bui AD, Henkel R (2018) Role of oxidative stress, infection and inflammation in male infertility. Andrologia 50(11):e13126

    Article  Google Scholar 

  2. Monteiro C, Marques PI, Cavadas B, Damião I, Almeida V, Barros N, Barros A, Carvalho F, Gomes S, Seixas S (2018) Characterization of microbiota in male infertility cases uncovers differences in seminal hyperviscosity and oligoasthenoteratozoospermia possibly correlated with increased prevalence of infectious bacteria. Am J Reprod Immunol 79(6):e12838

    Article  Google Scholar 

  3. Maldonado-Arriaga B, Escobar-Escamilla N, Pérez-Razo JC, Alcaráz-Estrada SL, Flores-Sánchez I, Moreno-García D, Pérez-Cabeza de Vaca R, Mondragón-Terán P, Shaw J, Hernandez-Cortez C, Castro-Escarpulli G, Suárez-Cuenca JA (2020) Mollicutes antibiotic resistance profile and presence of genital abnormalities in couples attending an infertility clinic. J Int Med Res 48(1):1–12

    Article  Google Scholar 

  4. Matorras R (2011) La infertilidad en España, sit-uación actual y perspectivas. 5th edn. Madrid. p. 19

  5. Qing L, Song QX, Feng JL, Li HY, Liu G, Jiang HH (2017) Prevalence of Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma genitalium and Ureaplasma urealyticum infections using a novel isothermal simultaneous RNA amplification testing method in infertile males. Ann Clin Microbiol Antimicrob 16(1):45

    Article  Google Scholar 

  6. Liang YY, Zhai HY, Li ZJ, Jin X, Chen Y, Chen SP (2019) Prevalence of Ureaplasma urealyticum, Chlamydia trachomatis, Neisseria gonorrhoeae and Herpes simplex virus in Beijing, China. Epidemiol Infect 147(e59):1–5

    Google Scholar 

  7. Park JJ, Seo YB, Jeong S, Lee J (2017) Prevalence of and risk factors for sexually transmitted infections among Korean adolescents under probation. J Korean Med Sci 32(11):1771–1778

    Article  Google Scholar 

  8. Sonmez C, Usluca S, Hakki Usluca I, Kalipci I, Sezen F, Resat Atalay C, Kilic S (2018) Evaluation of symptomatic patients with resistant discharge. Acta Dermatovenerol Croat 26(1):1–7

    CAS  PubMed  Google Scholar 

  9. Beeton ML, Payne MS, Jones L (2019) The role of Ureaplasma spp. in the development of nongonococcal urethritis and infertility among men. Clin Microbiol Rev 32(4):e00137–e00118

    Article  CAS  Google Scholar 

  10. Del Prete R, Ronga L, Lestingi M, Addati G, Angelotti UF, Di Carlo D, Miragliotta G (2017) Simultaneous detection and identification of STI pathogens by multiplex real-time PCR in genital tract specimens in a selected area of Apulia, a region of Southern Italy. Infection 45(4):469–477

    Article  Google Scholar 

  11. Huh HJ, Ki CS, Yun SA, Lee J, Oh GY, Lee NS, Yoon YH, Lee NY (2019) Comparison between DiaPlexQ™ STI6 and GeneFinder™ STD I/STD II multiplex real-time PCR kits in the detection of six sexually transmitted disease pathogens. J Clin Lab Anal 33(3):e22703

    Article  Google Scholar 

  12. Zhao L, Liu A, Li R, Zhao S (2019) Multiplex TaqMan real-time PCR platform for detection of Neisseria gonorrhoeae with decreased susceptibility to ceftriaxone. Diagn Microbiol Infect Dis 93(4):299–304

    Article  CAS  Google Scholar 

  13. Choi JB, Lee SJ, Lee MK, Lee SJ, Park DC, Kim HY, Lee DS, Choe HS (2018) Prevalence and antimicrobial susceptibility of Ureaplasma spp. and Mycoplasma hominis in asymptomatic individuals in Korea. Microb Drug Resist 24(9):1391–1396

    Article  CAS  Google Scholar 

  14. Foschi C, Salvo M, Galli S, Moroni A, Cevenini R, Marangoni A (2018) Prevalence and antimicrobial resistance of genital Mollicutes in Italy over a two-year period. New Microbiol 41(2):153–158

    CAS  PubMed  Google Scholar 

  15. Zhou YH, Ma HX, Yang Y, Gu WM (2018) Prevalence and antimicrobial resistance of Ureaplasma spp. and Mycoplasma hominis isolated from semen samples of infertile men in Shanghai, China from 2011 to 2016. Eur J Clin Microbiol Infect Dis 37(4):729–734

    Article  CAS  Google Scholar 

  16. Beeton ML, Spiller OB (2017) Antibiotic resistance among Ureaplasma spp. isolates: cause for concern? J Antimicrob Chemother 72(2):330–337

    Article  CAS  Google Scholar 

  17. Schneider SC, Tinguely R, Droz S, Hilty M, Donà V, Bodmer T, Endimiani A (2015) Antibiotic susceptibility and sequence type distribution of Ureaplasma species isolated from genital samples in Switzerland. Antimicrob Agents Chemother 59(10):6026–6031

    Article  CAS  Google Scholar 

  18. Zhang J, Kong Y, Feng Y, Huang J, Song T, Ruan Z, Song J, Jiang Y, Yu Y, Xie X (2014a) Development of a multilocus sequence typing scheme for Ureaplasma. Eur J Clin Microbiol Infect Dis 33(4):537–544

    Article  CAS  Google Scholar 

  19. Zhang J, Kong Y, Ruan Z, Huang J, Song T, Song J, Jiang Y, Yu Y, Xie X (2014b) Correlation between Ureaplasma subgroup 2 and genitourinary tract disease outcomes revealed by an expanded multilocus sequence typing (eMLST) scheme. PLoS One 9(8):e104347

    Article  Google Scholar 

  20. Yang T, Zou Y, Zhou W, Ruan Z, Kong Y, Zhou Y, Zhang J, Xie X (2018) Clonal diversity of Ureaplasma species and its relationship with oligozoospermia and semen quality in Chinese infertile males. Eur J Clin Microbiol Infect Dis 37(10):1957–1963

    Article  Google Scholar 

  21. Waites KB, Bade DJ, Bébéar C, Brown SD, Davidson MK, Duffy LB, Kenny G, Matlow A, Shortridge D, Talkington D, Totten PA, Watts JL, Zheng X (2011) Clinical and laboratory standards institute. M43-A, 31(19). Wayne (PA): Methods for antimicrobial susceptibility testing for human mycoplasmas; approved guideline

  22. Mardassi BB, Aissani N, Moalla I, Dhahri D, Dridi A, Mlik B (2012) Evidence for the predominance of a single tet(M) gene sequence type in tetracycline-resistant Ureaplasma parvum and Mycoplasma hominis isolates from Tunisian patients. J Med Microbiol 61(Pt 9):1254–1261

    Article  Google Scholar 

  23. Fernández J, Karau MJ, Cunningham SA, Greenwood-Quaintance KE, Patel R (2016) Antimicrobial susceptibility and clonality of clinical Ureaplasma isolates in the United States. Antimicrob Agents Chemother 60(8):4793–4798

    Article  Google Scholar 

  24. Beeton ML, Chalker VJ, Maxwell NC, Kotecha S, Spiller OB (2009) Concurrent titration and determination of antibiotic resistance in Ureaplasma species with identification of novel point mutations in genes associated with resistance. Antimicrob Agents Chemother 53(5):2020–2027

    Article  CAS  Google Scholar 

  25. Yang T, Pan L, Wu N, Wang L, Liu Z, Kong Y, Ruan Z, Xie X, Zhang J (2020) Antimicrobial resistance in clinical Ureaplasma spp. and mycoplasma hominis and structural mechanisms underlying quinolone resistance. Antimicrob Agents Chemother 64(6):e02560–e02519

    Article  Google Scholar 

  26. Valentine-King MA, Brown MB (2017) Antibacterial resistance in Ureaplasma species and Mycoplasma hominis isolates from urine cultures in college-aged females. Antimicrob Agents Chemother 61(10):e01104–e01117

    Article  CAS  Google Scholar 

  27. Govender S, Gqunta K, le Roux M, de Villiers B, Chalkley LJ (2012) Antibiotic susceptibilities and resistance genes of Ureaplasma parvum isolated in South Africa. J Antimicrob Chemother 67(12):2821–2824

    Article  CAS  Google Scholar 

  28. Piccinelli G, Gargiulo F, Biscaro V, Caccuri F, Caruso A, De Francesco MA (2017) Analysis of mutations in DNA gyrase and topoisomerase IV of Ureaplasma urealyticum and Ureaplasma parvum serovars resistant to fluoroquinolones. Infect Genet Evol 47:64–67

    Article  CAS  Google Scholar 

  29. Xiao L, Crabb DM, Duffy LB, Paralanov V, Glass JI, Waites KB (2012) Chromosomal mutations responsible for fluoroquinolone resistance in Ureaplasma species in the United States. Antimicrob Agents Chemother 56(5):2780–2783

    Article  CAS  Google Scholar 

  30. Ruan Z, Yang T, Shi X, Kong Y, Xie X, Zhang J (2017) Clonality and distribution of clinical Ureaplasma isolates recovered from male patients and infertile couples in China. PLoS One 12(8):e0183947

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank the laboratory staff of the Daan Gene Inc. for their help regarding the laboratory methodology.

Funding

This work was supported by the grants from the Projects of Medical and Health Technology Development Program in Shandong Province of China (grant no. 2017WS175) and Natural Science Foundation of Shandong Province of China (grant no. ZR2016HL44).

Author information

Authors and Affiliations

  1. Department of Laboratory, Tai’an Central Hospital, Tai’an, 271000, China

    Lihong Zhao & Shuping Zhao

  2. Central Laboratory, Tai’an Central Hospital, Tai’an, 271000, China

    Aihua Liu

  3. Department of Gynaecology, Tai’an Central Hospital, Tai’an, 271000, China

    Ruiying Li

Authors
  1. Lihong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aihua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruiying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuping Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shuping Zhao.

Ethics declarations

All the experiments undertaken in this study comply with the current law of the country where they were performed.

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, L., Liu, A., Li, R. et al. Antimicrobial resistance, genetic characterization, and molecular epidemiology of Ureaplasma species in males with infertility. Eur J Clin Microbiol Infect Dis 39, 2177–2183 (2020). https://doi.org/10.1007/s10096-020-03969-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-020-03969-7

Keywords

Search

Navigation